Previous Article | Next Article 
Molecular and Cellular Biology, September 1999, p. 6012-6019, Vol. 19, No. 9
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Base Pairing between U3 Small Nucleolar RNA and the
5' End of 18S rRNA Is Required for Pre-rRNA Processing
Kishor
Sharma1 and
David
Tollervey1,2,*
1European Molecular Biology Laboratory, Gene
Expression Programme, 69012 Heidelberg,
Germany, and 2 Institute of Cell and Molecular
Biology, University of Edinburgh, Edinburgh EH9 3JR, United
Kingdom
Received 15 March 1999/Returned for modification 23 April
1999/Accepted 28 May 1999
The loop of a stem structure close to the 5' end of the 18S rRNA is
complementary to the box A region of the U3 small nucleolar RNA
(snoRNA). Substitution of the 18S loop nucleotides inhibited pre-rRNA
cleavage at site A1, the 5' end of the 18S rRNA, and at
site A2, located 1.9 kb away in internal transcribed spacer 1. This inhibition was largely suppressed by a compensatory mutation in
U3, demonstrating functional base pairing. The U3-pre-rRNA base
pairing is incompatible with the structure that forms in the mature 18S
rRNA and may prevent premature folding of the pre-rRNA. In the
Escherichia coli pre-rRNA the homologous region of the 16S
rRNA is also sequestered, in that case by base pairing to the 5'
external transcribed spacer (5' ETS). Cleavage at site A0
in the yeast 5' ETS strictly requires base pairing between U3 and a
sequence within the 5' ETS. In contrast, the U3-18S interaction is not
required for A0 cleavage. U3 therefore carries out at least two functionally distinct base pair interactions with the pre-rRNA. The
nucleotide at the site of A1 cleavage was shown to be
specified by two distinct signals; one of these is the stem-loop
structure within the 18S rRNA. However, in contrast to the efficiency
of cleavage, the position of A1 cleavage is not dependent
on the U3-loop interaction. We conclude that the 18S stem-loop
structure is recognized at least twice during pre-rRNA processing.
*
Corresponding author. Mailing address: Institute of Cell and
Molecular Biology, University of Edinburgh, King's Buildings, Edinburgh EH9 3JR, United Kingdom. Phone: 44 131 650 7092. Fax: 44 131 650 7040. E-mail: d.tollervey{at}ed.ac.uk.
Molecular and Cellular Biology, September 1999, p. 6012-6019, Vol. 19, No. 9
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Lundkvist, P., Jupiter, S., Segerstolpe, A., Osheim, Y. N., Beyer, A. L., Wieslander, L.
(2009). Mrd1p Is Required for Release of Base-Paired U3 snoRNA within the Preribosomal Complex. Mol. Cell. Biol.
29: 5763-5774
[Abstract]
[Full Text]
-
Liang, X.-h., Liu, Q., Fournier, M. J.
(2009). Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. RNA
15: 1716-1728
[Abstract]
[Full Text]
-
Kent, T., Lapik, Y. R., Pestov, D. G.
(2009). The 5' external transcribed spacer in mouse ribosomal RNA contains two cleavage sites. RNA
15: 14-20
[Abstract]
[Full Text]
-
Segerstolpe, A., Lundkvist, P., Osheim, Y. N., Beyer, A. L., Wieslander, L.
(2008). Mrd1p binds to pre-rRNA early during transcription independent of U3 snoRNA and is required for compaction of the pre-rRNA into small subunit processomes. Nucleic Acids Res
36: 4364-4380
[Abstract]
[Full Text]
-
Goldfeder, M. B., Oliveira, C. C.
(2008). Cwc24p, a Novel Saccharomyces cerevisiae Nuclear Ring Finger Protein, Affects Pre-snoRNA U3 Splicing. J. Biol. Chem.
283: 2644-2653
[Abstract]
[Full Text]
-
Chakrabarti, K., Pearson, M., Grate, L., Sterne-Weiler, T., Deans, J., Donohue, J. P., Ares, M. Jr
(2007). Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA
13: 1923-1939
[Abstract]
[Full Text]
-
Perez-Fernandez, J., Roman, A., De Las Rivas, J., Bustelo, X. R., Dosil, M.
(2007). The 90S Preribosome Is a Multimodular Structure That Is Assembled through a Hierarchical Mechanism. Mol. Cell. Biol.
27: 5414-5429
[Abstract]
[Full Text]
-
Clery, A., Senty-Segault, V., Leclerc, F., Raue, H. A., Branlant, C.
(2007). Analysis of Sequence and Structural Features That Identify the B/C Motif of U3 Small Nucleolar RNA as the Recognition Site for the Snu13p-Rrp9p Protein Pair. Mol. Cell. Biol.
27: 1191-1206
[Abstract]
[Full Text]
-
Liang, X.-h., Fournier, M. J.
(2006). The Helicase Has1p Is Required for snoRNA Release from Pre-rRNA. Mol. Cell. Biol.
26: 7437-7450
[Abstract]
[Full Text]
-
Borovjagin, A. V., Gerbi, S. A.
(2005). An evolutionary intra-molecular shift in the preferred U3 snoRNA binding site on pre-ribosomal RNA. Nucleic Acids Res
33: 4995-5005
[Abstract]
[Full Text]
-
Vos, H. R., Bax, R., Faber, A. W., Vos, J. C., Raue, H. A.
(2004). U3 snoRNP and Rrp5p associate independently with Saccharomyces cerevisiae 35S pre-rRNA, but Rrp5p is essential for association of Rok1p. Nucleic Acids Res
32: 5827-5833
[Abstract]
[Full Text]
-
Gerczei, T., Correll, C. C.
(2004). Imp3p and Imp4p mediate formation of essential U3-precursor rRNA (pre-rRNA) duplexes, possibly to recruit the small subunit processome to the pre-rRNA. Proc. Natl. Acad. Sci. USA
101: 15301-15306
[Abstract]
[Full Text]
-
Gallagher, J. E.G., Dunbar, D. A., Granneman, S., Mitchell, B. M., Osheim, Y., Beyer, A. L., Baserga, S. J.
(2004). RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev.
18: 2506-2517
[Abstract]
[Full Text]
-
BOROVJAGIN, A. V., GERBI, S. A.
(2004). Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction. RNA
10: 942-953
[Abstract]
[Full Text]
-
YADAVA, R. S., MAHEN, E. M., FEDOR, M. J.
(2004). Kinetic analysis of ribozyme-substrate complex formation in yeast. RNA
10: 863-879
[Abstract]
[Full Text]
-
Atzorn, V., Fragapane, P., Kiss, T.
(2004). U17/snR30 Is a Ubiquitous snoRNA with Two Conserved Sequence Motifs Essential for 18S rRNA Production. Mol. Cell. Biol.
24: 1769-1778
[Abstract]
[Full Text]
-
Saijou, E., Fujiwara, T., Suzaki, T., Inoue, K., Sakamoto, H.
(2004). RBD-1, a nucleolar RNA-binding protein, is essential for Caenorhabditis elegans early development through 18S ribosomal RNA processing. Nucleic Acids Res
32: 1028-1036
[Abstract]
[Full Text]
-
Leary, D. J., Terns, M. P., Huang, S.
(2004). Components of U3 snoRNA-containing Complexes Shuttle between Nuclei and the Cytoplasm and Differentially Localize in Nucleoli: Implications for Assembly and Function. Mol. Biol. Cell
15: 281-293
[Abstract]
[Full Text]
-
Kufel, J., Allmang, C., Verdone, L., Beggs, J., Tollervey, D.
(2003). A complex pathway for 3' processing of the yeast U3 snoRNA. Nucleic Acids Res
31: 6788-6797
[Abstract]
[Full Text]
-
Sansam, C. L., Wells, K. S., Emeson, R. B.
(2003). Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc. Natl. Acad. Sci. USA
100: 14018-14023
[Abstract]
[Full Text]
-
Granneman, S., Gallagher, J. E. G., Vogelzangs, J., Horstman, W., Venrooij, W. J. v., Baserga, S. J., Pruijn, G. J. M.
(2003). The human Imp3 and Imp4 proteins form a ternary complex with hMpp10, which only interacts with the U3 snoRNA in 60-80S ribonucleoprotein complexes. Nucleic Acids Res
31: 1877-1887
[Abstract]
[Full Text]
-
Chen, W., Bucaria, J., Band, D. A., Sutton, A., Sternglanz, R.
(2003). Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res
31: 690-699
[Abstract]
[Full Text]
-
Granneman, S., Pruijn, G. J. M., Horstman, W., van Venrooij, W. J., Luhrmann, R., Watkins, N. J.
(2002). The hU3-55K Protein Requires 15.5K Binding to the Box B/C Motif as Well as Flanking RNA Elements for Its Association with the U3 Small Nucleolar RNA in Vitro. J. Biol. Chem.
277: 48490-48500
[Abstract]
[Full Text]
-
Wehner, K. A., Gallagher, J. E. G., Baserga, S. J.
(2002). Components of an Interdependent Unit within the SSU Processome Regulate and Mediate Its Activity. Mol. Cell. Biol.
22: 7258-7267
[Abstract]
[Full Text]
-
Borovjagin, A. V., Gerbi, S. A.
(2001). Xenopus U3 snoRNA GAC-Box A' and Box A Sequences Play Distinct Functional Roles in rRNA Processing. Mol. Cell. Biol.
21: 6210-6221
[Abstract]
[Full Text]
-
GERBI, S.A., BOROVJAGIN, A.V., EZROKHI, M., LANGE, T.S.
(2001). Ribosome Biogenesis: Role of Small Nucleolar RNA in Maturation of Eukaryotic rRNA. Cold Spring Harb Symp Quant Biol
66: 575-590
[Abstract]
-
Speckmann, W. A., Terns, R. M., Terns, M. P.
(2000). The Box C/D motif directs snoRNA 5'-cap hypermethylation. Nucleic Acids Res
28: 4467-4473
[Abstract]
[Full Text]
-
Colley, A., Beggs, J. D., Tollervey, D., Lafontaine, D. L. J.
(2000). Dhr1p, a Putative DEAH-Box RNA Helicase, Is Associated with the Box C+D snoRNP U3. Mol. Cell. Biol.
20: 7238-7246
[Abstract]
[Full Text]
-
Schnare, M. N., Collings, J. C., Spencer, D. F., Gray, M. W.
(2000). The 28S-18S rDNA intergenic spacer from Crithidia fasciculata: repeated sequences, length heterogeneity, putative processing sites and potential interactions between U3 small nucleolar RNA and the ribosomal RNA precursor. Nucleic Acids Res
28: 3452-3461
[Abstract]
[Full Text]
-
Kufel, J., Allmang, C., Chanfreau, G., Petfalski, E., Lafontaine, D. L. J., Tollervey, D.
(2000). Precursors to the U3 Small Nucleolar RNA Lack Small Nucleolar RNP Proteins but Are Stabilized by La Binding. Mol. Cell. Biol.
20: 5415-5424
[Abstract]
[Full Text]
-
Antal, M., Mougin, A., Kis, M., Boros, E., Steger, G., Jakab, G., Solymosy, F., Branlant, C.
(2000). Molecular characterization at the RNA and gene levels of U3 snoRNA from a unicellular green alga, Chlamydomonas reinhardtii. Nucleic Acids Res
28: 2959-2968
[Abstract]
[Full Text]
-
Speckmann, W., Narayanan, A., Terns, R., Terns, M. P.
(1999). Nuclear Retention Elements of U3 Small Nucleolar RNA. Mol. Cell. Biol.
19: 8412-8421
[Abstract]
[Full Text]